Person:

Lieberman, Daniel

Endurance running (ER) poses a conundrum for paleoanthropologists. As summarized in Bramble and Lieberman (2004), human ER capabilities, which are unique among primates, either match or exceed those of mammals adapted for running (cursors), including dogs and equids. Because many of the biomechanical and physiological challenges of human ER are so different from those of walking, we can conclude that human ER capabilities did not arise merely as a by-product of selection for walking. Instead, the available evidence suggests that an array of features that improve ER performance were selected in the genus Homo, and they were probably present to some extent by the appearance of Homo erectus at approximately 1.9 Ma. Yet, ER is no longer necessary for human survival, even among extant foragers such as the Hadza or the Bushmen. Thus, a puzzle that paleoanthropologists must solve is identifying what past behaviors - behaviors no longer common among living foragers - favored the evolution of ER. Pickering and Bunn’s (2007) criticisms of the ER hypothesis center on two issues: first, that early Homo lacked the tracking abilities necessary for successful pursuit hunts, and second, that recent ethnographic evidence suggests that modern hunter-gatherers rarely use ER to either hunt or scavenge. These arguments are based on a presumptive link between modern human- like cognition and tracking abilities, as well as the notion that the modern ethnographic record provides an adequate reflection of past behaviors. Both of these assumptions are flawed. Although tracking is complex, there is little evidence to suggest that early hominids lacked the tracking abilities of much less encephalized carnivores. Additionally, as noted by Marlowe (2005), comparatively recent inventions, such as the bow and arrow, the spear thrower, nets, and even the spear point, fundamentally altered how humans hunt and scavenge. A strict reliance on the recent ethnographic record, what Wobst (1978) termed the ‘‘tyranny of ethnography,’’ is a fundamentally problematic way of testing hypotheses of past hunting behavior. Even so, a review of the ethnographic evidence reveals errors in Pickering and Bunn’s contentions.

The human gluteus maximus is a distinctive muscle in terms of size, anatomy and function compared to apes and other non-human primates. Here we employ electromyographic and kinematic analyses of human subjects to test the hypothesis that the human gluteus maximus plays a more important role in running than walking. The results indicate that the gluteus maximus is mostly quiescent with low levels of activity during level and uphill walking, but increases substantially in activity and alters its timing with respect to speed during running. The major functions of the gluteus maximus during running are to control flexion of the trunk on the stanceside and to decelerate the swing leg; contractions of the stance-side gluteus maximus may also help to control flexion of the hip and to extend the thigh. Evidence for when the gluteus maximus became enlarged in human evolution is equivocal, but the muscle’s minimal functional role during walking supports the hypothesis that enlargement of the gluteus maximus was likely important in the evolution of hominid running capabilities.

Integration, a fundamental property of organisms, occurs via multiple mechanisms and for diverse reasons. Although there has been substantial work on the genetic and epigenetic mechanisms by which developmental integration occurs, we have less of an understanding of the evolutionary relationships between functional and developmental integration. In this respect, human evolution provides an interesting test case. In quadrupedal mammals, there is considerable functional integration among and between the limbs, but little functional integration between the limbs and the skull. The evolution of bipedalism in hominids, however, provided new opportunities for novel forms of integration by emancipating the forelimbs from any major role in locomotion. Here we consider how the forelimb and head become increasingly integrated in the genus Homo because of the biomechanical challenges of running. While the arm and the head interact little during walking, we have found that, during running, the stance side arm acts as a counterbalance to the head, stabilizing it against impulsive pitching forces generated by the heel strike transient. Moreover, the functional properties of this linkage may have driven several developmental changes in the proportions of the arm and the anatomy of the shoulder girdle during human evolution. Thus, evolutionary changes in arm and head morphology during human evolution may be more integrated than previously considered.

Humans habitually swing their arms in phase with the contralateral leg during walking and running. This arm motion is generally thought to counteract the torque about the body’s vertical axis (i.e. yaw moment) that is generated by the legs as they swing with each step. Thus it has been argued that the motion of the arms is a tuned, habitual, active response that is critical for maintaining stability during human locomotion, especially running. In this study, we investigated whether arm swing is in fact an active behavior, or is instead a passive response that follows solely as a consequence of our anatomical design. Human subjects walked and ran on a treadmill under different arm- and leg-weighting conditions, and without armswing, while kinematic and surface EMG data were recorded. A modeling study was also performed to determine the inherent effect of leg swing on arm movement in a human-like biped. Results of both studies suggest that arm swing is largely a passive response, and is not entirely an active, tuned behavior. Arm swing may therefore be an emergent property of human bipedalism, with the arms acting largely as passive damping mechanisms that decrease whole-body yawing.

One of the most distinctive features of humans relative to other apes is a greatly expanded gluteus maximus. We examined the role of this muscle in walking and running humans to test the hypothesis that the derived expansion of the gluteus maximus may be related to various musculoskeletal specifications for endurance running. During a walk, the trunk is relatively vertical, positioning the upper body’s center of gravity over the hip joint: during a run, the trunk is more forwardly inclined, with the upper body’s center of gravity well in front of the hip joint. This inclination causes the trunk to have an inertial tendency to pitch forward at foot strike. Although the gluteus is well know to be a hip extensor, its contraction will also counteract pitching of the trunk when the leg is on the ground. The hypothesis was tested using EMG and kinematic analysis of human subjects during walking and running under various conditions. The results indicate that the gluteus maximus contracts bilaterally at foot strike during running but not walking. On the stance side, the gluteus maximus functions to stabilize the trunk against its inertial tendency to pitch at foot strike. On the swing side, the gluteus maximus may contract to help decelerate the leg prior to foot strike. Presence of an enlarged surface of attachment for this muscle in Homo erectus suggests that the expansion of this muscle may have played an influential role in early human endurance running capabilities.

Integration, a fundamental property of organisms, occurs via multiple mechanisms and for diverse reasons. Although there has been substantial work on the genetic and epigenetic mechanisms by which developmental integration occurs, we have less of an understanding of the evolutionary relationships between functional and developmental integration. In this respect, human evolution provides an interesting test case. In quadrupedal mammals, there is considerable functional integration among and between the limbs, but less integration between the limbs and the head. The evolution of bipedalism in hominins, however, provided a new opportunities for novel forms of integration by emancipating the forelimbs from any major role in locomotion. Here we consider how the forelimb and head become increasingly integrated in the genus Homo because of the biomechanical challenges of running. While the arm and the head interact little during walking, we have found that, during running, the stance side arm acts as a counterbalance to the head, stabilizing it against impulsive pitching forces generated by the heel strike transient. Moreover, the functional properties of this linkage may have driven several developmental changes in the proportions of the arm and the anatomy of the shoulder girdle during human evolution. Thus, evolutionary changes in arm and head morphology during human evolution may be more integrated than previously considered. This work was supported by funding from NFS.

We investigated the control and function of arm swing in human walking and running to test the hypothesis that the arms act as passive mass dampers powered by movement of the lower body, rather than being actively driven by the shoulder muscles. We measured locomotor cost, deltoid muscle activity and kinematics in 10 healthy adult subjects while walking and running on a treadmill in three experimental conditions: control; no arms (arms folded across the chest); and arm weights (weights worn at the elbow). Decreasing and increasing the moment of inertia of the upper body in no arms and arm weights conditions, respectively, had corresponding effects on head yaw and on the phase differences between shoulder and pelvis rotation, consistent with the view of arms as mass dampers. Angular acceleration of the shoulders and arm increased with torsion of the trunk and shoulder, respectively, but angular acceleration of the shoulders was not inversely related to angular acceleration of the pelvis or arm. Restricting arm swing in no arms trials had no effect on locomotor cost. Anterior and posterior portions of the deltoid contracted simultaneously rather than firing alternately to drive the arm. These results support a passive arm swing hypothesis for upper body movement during human walking and running, in which the trunk and shoulders act primarily as elastic linkages between the pelvis, shoulder girdle and arms, the arms act as passive mass dampers which reduce torso and head rotation, and upper body movement is primarily powered by lower body movement.

Humans experience relatively high ground impact forces during running that can destabilize the head, especially at heel strike. Although head pitch is by far the largest challenge, an appreciable degree of roll also occurs (as is evident when a runner’s pony-tailed hair swings recurrently from side to side). Here we analyze the kinematic and kinetic forces of head roll and how the body stabilizes angular accelerations in the coronal plane. At endurance running speeds, the head rolls towards the stance side approaching 50s-1, reaching peak rates near midstance, well after the time of peak pitching rates. Our analysis identifies a roll mediating mechanism in activation of the swing side sternocleidomastoid muscle (SCM) just before heel strike followed by a peak magnitude burst of the muscle some 40-80ms before the head attains peak roll rate. The SCM fires on the stance side as well but with much shorter duration and lower magnitude, suggesting that the increased activity of the swing side SCM functions in head roll control. There is no apparent correspondence of unilateral activity of the cranial and cervical trapezius muscles with head roll.

Mammals must stabilize the head during running to keep angular accelerations of head within the operating range of the vestibulo-ocular (VOR) reflexes. However, several unique aspects of the human body plan and locomotor kinematics make head stabilization more challenging than in other cursors. Most bipedal and quadrupedal cursors have cantilevered heads and necks that act to attenuate forces and counter sagittal head pitching through controlled flexion and extension movements. In contrast, humans have short vertical necks that emerge from near center of head, combined with relatively extended, stiff legs at heel strike (HS), resulting in a strong tendency for the head to pitch forward at the beginning of stance. Using EMG, kinematic, and kinetic measurements of human arm and head movements during running and walking we show that humans stabilize the head following HS using a unique tuned-mass damper system. This mechanism, which links the head with inertial forces in the stance side (ipsilateral) arm, is facilitated by a number of derived aspects of human anatomy and running kinematics. Notably, humans have lost all muscular connections between shoulder girdle and head except for the cleidocranial portion of the trapezius (CCT), which reaches the occiput via a tendon-like nuchal ligament. Additionally, coordinated movements of the arm and thorax position the ipsilateral arm behind the head-neck joint prior to HS, when the ipsilateral CCT fires. Out of phase accelerations of the arm and head then link the counterbalancing mass of the arm and the flexed forearm via a compliant connection to the head, controlling the head’s rate of pitch. Because the nuchal ligament, a key component of the system, leaves a trace on the skull, it is possible to show that this novel mechanism for head stabilization originated within the genus Homo approximately 2 millions years ago.